Diversity of fungus‐growing termites (Macrotermes) and their fungal symbionts (Termitomyces) in the semiarid Tsavo Ecosystem,Kenya

Fungus‐growing termites of the subfamily Macrotermitinae together with their highly specialized fungal symbionts (Termitomyces) are primary decomposers of dead plant matter in many African savanna ecosystems. The termites provide crucial ecosystem services also by modifying soil properties, translocating nutrients, and as important drivers of plant succession. Despite their obvious ecological importance, many basic features in the biology of fungus‐growing termites and especially their fungal symbionts remain poorly known, and no studies have so far focused on possible habitat‐level differences in symbiont diversity across heterogeneous landscapes. We studied the species identities of Macrotermes termites and their Termitomyces symbionts by excavating 143 termite mounds at eight study sites in the semiarid Tsavo Ecosystem of southern Kenya. Reference specimens were identified by sequencing the COI region from termites and the ITS region from symbiotic fungi. The results demonstrate that the regional Macrotermes community in Tsavo includes two sympatric species (M. subhyalinus and M. michaelseni) which cultivate and largely share three species of Termitomyces symbionts. A single species of fungus is always found in each termite mound, but even closely adjacent colonies of the same termite species often house evolutionarily divergent fungi. The species identities of both partners vary markedly between sites, suggesting hitherto unknown differences in their ecological requirements. It is apparent that both habitat heterogeneity and disturbance history can influence the regional distribution patterns of both partners in symbiosis.     

Importance ofCubitermes termitaries as shelter for alien incipient termite societies

Summary We hypothetized that in the African rainforest (Cameroon), one of the principal limiting factors for termite multiplication is the relative scarcity of nesting sites. As a consequence, termitaries ofCubitermes fungifaber, C. banksi andC. subarquatus with their alveolate structure might constitute good shelters for incipient societies. In the cavities of these termitaries we recorded 29 termite species (including conspecifics) belonging to 23 genera and 5 subfamilies.ActiveCubitermes fungifaber andC. banksi termitaries shelter fewer incipient and adult societies than abandoned ones. ActiveC. subarquatus termitaries shelter more incipient societies than abandoned ones, while the difference is not significant with regards to termite societies at other stages of development.The frequency of shelteredCubitermes spp. incipient societies was so large (72.3%) that we suggest that abandoned termitaries and unoccupied zones of active ones had an adaptative value at the generic level as they constitute good shelters (probably the best) for incipient societies and favour reproduction inCubitermes spp. societies.     

Differences in feeding behaviour among Chironomus species revealed by measurements of sulphur stable isotopes and cadmium in larvae

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Forest refugia and riverine barriers promote diversification in the West African pygmy shrew (Crocidura obscurior complex,Soricomorpha)

The Crocidura obscurior or West African pygmy shrew complex is endemic to West African forests from south‐eastern Guinea, eastern Liberia, southern Côte d'Ivoire and south‐western Ghana. We explore the genetic and morphometric diversity of 239 individuals of the C. obscurior complex from 17 localities across its geographical range. Using genetic data from three mitochondrial (16S, cytochrome b and COI) and four nuclear markers (BRCA1, STAT5A, HDAC2 and RIOK3) and skull geometric morphometrics, we show that this complex is composed of two cryptic and sympatric species, C. obscurior and C. eburnea. We then test several hypotheses to infer their evolutionary history. The observed phylogeographical pattern based on cytochrome b and COI sequences fits the forest refuge theory: during arid phases of the Plio‐Pleistocene, around 3.5, 2.1, 1 and 0.5 Mya, a small number of populations survived in isolated forest patches and diverged allopatrically. During wetter climatic periods, forests expanded, leading to secondary contacts between previously isolated populations. Our results also suggest the possible contribution of episodes of isolation in subrefuges. Historical variation of the West African hydrographic network could also have contributed to the observed patterns of genetic differentiation. Rivers such as the Volta and Sassandra may act as past and/or current barriers to gene flow. Although these two species have sympatric distributions, their phylogeographical histories are somewhat dissimilar due to small differences in their dispersal abilities and ecological requirements.     

Characterization of a laccase from a wood‐feeding termite,Coptotermes formosanus

Coptotermes formosanus Shiraki is a wood‐feeding termite which secretes a series of lignolytic and cellulolytic enzymes for woody biomass degradation. However, the lignin modification mechanism in the termite is largely elusive, and the characteristics of most lignolytic enzymes in termites remain unknown. In this study, a laccase gene lac1 from C. formosanus was heterogeneously expressed in insect Sf9 cells. The purified Lac1 showed strong activities toward hydroquinone (305 mU/mg) and 2,6‐dimethoxyphenol (2.9 mU/mg) with low K_m values, but not veratryl alcohol or 2,2’‐azino‐bis (3‐ethylbenzothiazoline‐6‐sulfonic acid). Lac1 could function well from pH 4.5 to 7.5, and its activity was significantly inhibited by H₂O₂ at above 4.85 mmol/L (P < 0.01). In addition, the lac1 gene was found to be mainly expressed in the salivary glands and foregut of C. formosanus, and seldom in the midgut or hindgut. These findings suggested that Lac1 is a phenol‐oxidizing laccase like RflacA and RflacB from termite Reticulitermes flavipes, except that Lac1 was found to be more efficient in phenol oxidation, and it did not require H₂O₂ for its function. It is suspected that this kind of termite laccase might only be able to directly oxidize low redox‐potential substrates, and the high redox‐potential groups in lignin might be oxidized by other enzymes in the termite or by using the Fenton reaction.     

Termite diversity in Neotropical dry forests of Colombia and the potential role of rainfall in structuring termite diversity

Termites are ecosystem engineers that play an important role in the biotransformation and re‐distribution of nutrients in soil. The dry forests are endemic repositories, but at same time, they are most threatened by extensive livestock and crop farming, fires, and climate change. In Colombia, the best‐protected dry forests are located in the north. The termite fauna of dry forests are poorly known. The aim was to identify the termite species occurring in tropical dry forests of the Colombian Caribbean coast in relation to diet and precipitation, temperature, elevation, and soil properties. A total of 32 species in 1,103 occurrences were found. Termitidae accounted for 78% of the species richness with the Anoplotermes‐group, Microcerotermes, and Nasutitermes being the dominant genera. Differences in species composition and abundance were found across sites. These differences may be linked to anthropogenic disturbance and polygyny and polydomy. Strikingly, our highest elevation site (334 m) had the highest species richness much higher than the two lower elevation sites. This implies an inversion of the common elevation‐diversity gradient, also found for termites which can be explained by increasing precipitation with elevation in the dry forest. An analysis of termite species richness at the global scale confirms that termite species richness correlates positively with rainfall. Hence, rainfall seems to positively affect termite diversity. In line, the studied Colombian tropical dry forests had low diversity compared to rain forests. A decline of species‐rich soil‐feeding termites with increasing aridity may explain why the highest termite diversity occurs in humid tropical rain forests. Abstract in Spanish is available with online material.     

Utilizing rabbit immunoglobulin G protein for mark-capture studies on the desert subterranean termite, Heterotermes aureus (Snyder)

Mark-capture dispersal studies were conducted to investigate the feasibility of marking the southwestern desert subterranean termite, Heterotermes aureus (Snyder) with rabbit immunoglobulin G (IgG). In turn, short-range dispersal patterns of H. aureus were measured across a 20-m diameter desert landscape at three distinct field locations. Each location consisted of 51 termite feeding stations containing corrugated cardboard. The central feeding station (CFS) at each location was impregnated with rabbit IgG. A circular grid was then constructed around each CFS that consisted of 50 additional unmarked cardboard feeding stations strategically placed around the CFS at distances of 1.5, 2.0, 4.0, 7.0 or 10.0 m. Termites self-marked with rabbit IgG by feeding on the marked bait. The CFS and the 50 peripheral feeding stations were sampled for marked termites twice at each location 17–65 days after the marked bait was placed at the CFS to determine the spatial dispersal patterns of H. aureus within each research grid. Termites that self marked by feeding on rabbit IgG marked bait were detected by an anti-rabbit IgG enzyme-linked immunosorbent assay (ELISA). Generally, the CFSs contained the highest frequency of marked termites with 28.0% of the individuals assayed from the CFSs containing rabbit IgG. Over the course of the study, 39 of the unmarked peripheral feeding stations contained at least one marked termite. Of the termites assayed from the peripheral stations (n = 2,955), 124 or 4.2% of the individuals contained the mark. The average distance traveled by the marked termites collected at the peripheral feeding stations was 5.7 ± 3.3 m from the CFSs. We also examined single nucleotide polymorphisms (SNPs) from termites collected at each field site. Data indicated that each field site were genetically distinct and therefore non-related termites. We discuss the advantages and limitations of marking termites with rabbit IgG for dispersal studies.     

The trade‐off between fecundity and egg size in a polymorphic population of Arctic charr (Salvelinus alpinus (L.)) in Skogsfjordvatn,subarctic Norway

Reproductive traits differ between intralacustrine Arctic charr morphs. Here, we examine three sympatric lacustrine Arctic charr morphs with respect to fecundity, egg size and spawning time/site to assess reproductive investments and trade‐offs, and possible fitness consequences. The littoral omnivore morph (LO‐morph) utilizes the upper water for feeding and reproduction and spawn early in October. The large profundal piscivore morph (PP‐morph) and the small profundal benthivore morph (PB‐morph) utilize the profundal habitat for feeding and reproduction and spawn in December and November, respectively. Females from all morphs were sampled for fecundity and egg‐size analysis. There were large differences between the morphs. The PB‐morph had the lowest fecundity (mean = 45, SD = 13) and smallest egg size (mean = 3.2 mm, SD = 0.32 mm). In contrast, the PP‐morph had the highest fecundity (mean = 859.5, SD = 462) and the largest egg size (mean = 4.5 mm, SD = 0.46 mm), whereas the LO‐morph had intermediate fecundity (mean = 580, SD = 225) and egg size (mean = 4.3, SD = 0.24 mm). Fecundity increased with increasing body size within each morph. This was not the case for egg size, which was independent of body sizes within morph. Different adaptations to feeding and habitat utilization have apparently led to a difference in the trade‐off between fecundity and egg size among the three different morphs.     

Genetic signs of multiple colonization events in Baltic ciscoes with radiation into sympatric spring‐ and autumn‐spawners confined to early postglacial arrival

Presence of sympatric populations may reflect local diversification or secondary contact of already distinct forms. The Baltic cisco (Coregonus albula) normally spawns in late autumn, but in a few lakes in Northern Europe sympatric autumn and spring‐ or winter‐spawners have been described. So far, the evolutionary relationships and taxonomic status of these main life history forms have remained largely unclear. With microsatellites and mtDNA sequences, we analyzed extant and extinct spring‐ and autumn‐spawners from a total of 23 Swedish localities, including sympatric populations. Published sequences from Baltic ciscoes in Germany and Finland, and Coregonus sardinella from North America were also included together with novel mtDNA sequences from Siberian C. sardinella. A clear genetic structure within Sweden was found that included two population assemblages markedly differentiated at microsatellites and apparently fixed for mtDNA haplotypes from two distinct clades. All sympatric Swedish populations belonged to the same assemblage, suggesting parallel evolution of spring‐spawning rather than secondary contact. The pattern observed further suggests that postglacial immigration to Northern Europe occurred from at least two different refugia. Previous results showing that mtDNA in Baltic cisco is paraphyletic with respect to North American C. sardinella were confirmed. However, the inclusion of Siberian C. sardinella revealed a more complicated pattern, as these novel haplotypes were found within one of the two main C. albula clades and were clearly distinct from those in North American C. sardinella. The evolutionary history of Northern Hemisphere ciscoes thus seems to be more complex than previously recognized.     

Isolation and assessment of gut bacteria from the Formosan subterranean termite,Coptotermes formosanus (Isoptera: Rhinotermitidae), for paratransgenesis research and application

Paratransgenesis targeting the gut protozoa is being developed as an alternative method for the control of the Formosan subterranean termite (FST). This method involves killing the cellulose‐digesting gut protozoa using a previously developed antiprotozoal peptide consisting of a target specific ligand coupled to an antimicrobial peptide (Hecate). In the future, we intend to genetically engineer termite gut bacteria as “Trojan Horses” to express and spread ligand‐Hecate in the termite colony. The aim of this study was to assess the usefulness of bacteria strains isolated from the gut of FST as “Trojan Horses.” We isolated 135 bacteria from the guts of workers from 3 termite colonies. Sequencing of the 16S rRNA gene identified 20 species. We tested 5 bacteria species that were previously described as part of the termite gut community for their tolerance against Hecate and ligand‐Hecate. Results showed that the minimum concentration required to inhibit bacteria growth was always higher than the concentration required to kill the gut protozoa. Out of the 5 bacteria tested, we engineered Trabulsiella odontotermitis, a termite specific bacterium, to express green fluorescent protein as a proof of concept that the bacteria can be engineered to express foreign proteins. Engineered T. odontotermitis was fed to FST to study if the bacteria are ingested. This feeding experiment confirmed that engineered T. odontotermitis is ingested by termites and can survive in the gut for at least 48 h. Here we report that T. odontotermitis is a suitable delivery and expression system for paratransgenesis in a termite species.     

Hybridisation and introgression between Brassica napus and B. rapa in the Netherlands

We used flow cytometry, chromosome counting and AFLP markers to investigate gene flow from the crop plant oilseed rape, Brassica napus (AACC) to wild B. rapa (AA) in the Netherlands. From 89 B. napus source populations investigated, all near cropping fields or at transhipment sites, only 19 contained a B. rapa population within a 2.5‐km radius. During our survey we found only three populations with F1 hybrids (AAC), as recognized by their nine extra chromosomes and by flow cytometry. These hybrids were all collected in mixed populations where the two species grew in close proximity. Populations with F1 hybrids were not close to crops, but instead were located on road verges with highly disturbed soils, in which both species were probably recruited from the soil seed bank. Many plants in the F2, BC1 or higher backcrosses are expected to carry one to eight C chromosomes. However, these plants were not observed among the hybrids. We further investigated introgression with molecular markers (AFLP) and compared sympatric B. rapa populations (near populations of B. napus) with control populations of B. rapa (no B. napus within at least 7 km). We found no difference between sympatric and control populations in the number of C markers in B. rapa, nor did we find that these sympatric populations closely resembled B. napus. Our data show that hybrids occur but also suggest no recent introgression of alleles from the crop plant B. napus into wild B. rapa in the Dutch populations studied.     

Termite mound formation reduces the abundance and diversity of soil resistomes

Termites are pivotal ecosystem engineers in tropical and subtropical habitats, where they construct massive nests (‘mounds’) that substantially modify soil properties and promote nutrient cycling. Yet, little is known about the roles of termite nesting activity in regulating the spread of antimicrobial resistance (AMR), one of the major Global Health challenges. Here, we conducted a large-scale (> 1500 km) investigation in northern Australia and found distinct resistome profiles in termite mounds and bulk soils. By profiling a wide spectrum of ARGs, we found that the abundance and diversity of antibiotic resistance genes (ARGs) were significantly lower in termite mounds than in bulk soils (P < 0.001). The proportion of efflux pump ARGs was significantly lower in termite mound resistome than in bulk soil resistome (P < 0.001). The differences in resistome profiles between termite mounds and bulk soils may result from the changes in microbial interactions owing to the substantial increase in pH and nutrient availability induced by termite nesting activities. These findings advance our understanding of the profile of ARGs in termite mounds, which is a crucial step to evaluate the roles of soil faunal activity in regulating soil resistome under global environmental change.     

Sympatric wolf and coyote populations of the western Great Lakes region are reproductively isolated

Interpretation of the genetic composition and taxonomic history of wolves in the western Great Lakes region (WGLR) of the United States has long been debated and has become more important to their conservation given the recent changes in their status under the Endangered Species Act. Currently, the two competing hypotheses on WGLR wolves are that they resulted from hybridization between (i) grey wolves (Canis lupus) and western coyotes (C. latrans) or (ii) between grey wolves and eastern wolves (C. lycaon). We performed a genetic analysis of sympatric wolves and coyotes from the region to assess the degree of reproductive isolation between them and to clarify the taxonomic status of WGLR wolves. Based on data from maternal, paternal and bi‐parental genetic markers, we demonstrate a clear genetic distinction between sympatric wolves and coyotes and conclude that they are reproductively isolated and that wolf–coyote hybridization in the WGLR is uncommon. The data reject the hypothesis that wolves in the WGLR derive from hybridization between grey wolves and western coyotes, and we conclude that the extant WGLR wolf population is derived from hybridization between grey wolves and eastern wolves. Grey‐eastern wolf hybrids (C. lupus × lycaon) comprise a substantial population that extends across Michigan, Wisconsin, Minnesota and western Ontario. These findings have important implications for the conservation and management of wolves in North America, specifically concerning the overestimation of grey wolf numbers in the United States and the need to address policies for hybrids.     

Iron reduction in the metal-rich guts of wood-feeding termites

Termites play important roles in lignocellulose and humus turnover in diverse terrestrial ecosystems, and are significant sources of global atmospheric methane and carbon dioxide. All known termite species engage in obligate, complex nutritional symbioses with their gut microbes to carry out such processes. Several hundred microbial species, representing a broad phylogenetic and physiological diversity, are found within the well‐bounded, microliter‐in‐scale gut ecosystem of a given termite. However, most of these species have never been obtained in laboratory culture, and little can be said about their functional roles in the gut community or symbiosis. Herein, an unappreciated facet of the gut chemistry and microbiology of wood‐feeding termites is revealed: the redox metabolism of iron. Gut fluids from field‐collected termites contained millimolar amounts of ferrous iron and other heavy metals. When iron(III) hydroxides were amended to a filter paper diet of Zootermopsis nevadensis, a dampwood termite collected in the San Gabriel Mountains of Southern California, the specimens accumulated high levels of iron(II) in their guts. Additionally, iron was reduced at rapid initial rates in anoxic gut homogenates prepared from field‐collected Z. nevadensis specimens. A Clostridium sp. and a Desulfovibrio sp. were isolated from dilution‐to‐extinction enrichments of Z. nevadensis gut contents and were found to reduce iron(III), as did the termite gut spirochete Treponema primitia. The iron in the guts of wood‐feeding termites may influence the pathways of carbon‐ and electron‐flow, as well as microbial community composition in these tiny ecosystems of global importance.     

Effects of different food on growth and survival of first‐feeding taimen Hucho taimen (Pallas, 1773) larvae

A study was conducted to compare growth and survival of Hucho taimen larvae from 21 to 76 days after hatch (DAH) fed one of three diets: formulated feed alone (group F); a co‐feeding diet of water fleas, tubifex and formulated feed (group C); or live food of water fleas and tubifex (group L), and to investigate the potential use of dietary L‐alanyl‐L‐glutamine (L‐AG) in larval taimen for a more nutritious starter diet. Triplicate groups of 5000 fish were randomly assigned to each aquarium provided with water from a flow‐through system, and fed to apparent satiation. The results show that larvae can feed efficiently on floating crumbled particles of formulated feed. Weight gain of larvae fed only formulated feed was significantly lower than other groups at 34 DAH (P < 0.05). At the end of the experiment, weight gain reached the highest value in group F and was lowest in group L (P < 0.05). Condition factor reached the highest values in group F and lowest in group C (P < 0.05). Specific growth rate was in accordance with weight gain at 76 DAH. Survival showed no differences among the groups (P > 0.05). In conclusion, H. taimen larvae can be fed formulated feed alone and L‐AG may be used as a feeding attractant during the weaning process, which should lead to a better understanding in the rearing improvement in the feeding of larvae.     

Mate Choice by Both Sexes Maintains Reproductive Isolation in a Species Flock of Pupfish (Cyprinodon spp) in the Bahamas

Female and male mate choices can reinforce reproductive isolation after sympatric speciation. Using a binary choice design, we examine the importance of visual cues in female mate choice in all three sympatric species of pupfish on San Salvador Island. We also examine the importance of olfactory cues in female choice of the hard‐shelled invertebrate specialist (Cyprinodon brontotheroides). We examine male mate choice in two of the three species, the scale eater (C. desquamator) and the detritivore (C. variegatus). Females of all three species use visual cues and prefer conspecific males. C. brontotheroides females do not use olfactory cues to discriminate between conspecific and heterospecific males. Males of C. desquamator and C. variegatus also preferentially court conspecific females. Thus, mutual mate choice, where both females and males exhibit mate choice, acts as a strong behavioral pre‐mating isolation mechanism in these sympatrically speciated pupfish.     

Roost Structure,Modification, and Availability in the White‐throated Round‐eared Bat,Lophostoma silvicolum (Phyllostomidae) Living in Active Termite Nests1

We studied roost structure, modification, and availability in Lophostoma silvicolum (Phyllostomidae), an insectivorous gleaning bat, on Barro Colorado Island (BCI), Panamá. Collection of nest material beneath termitaria and infrared video filming indicated that males of L. silvicolum excavate and maintain cavities inside active termite nests. A binary logistic regression analysis showed that to be suitable as roosts, termite nests have to be larger than 30 cm in diameter and taller than 30 cm, well shaded, with few transecting branches, and freely accessible from below. Use of active termite nests as roosts may provide several benefits to L. silvicolum, including reduction of competition for roost sites with sympatric bat species, reduced parasite load and a suitable microclimate. A comparison of number of all termite nests in selected forest plots with number of termite nests that are potentially suited as bat roosts and number of termite nests that are actually used by bats suggests that L. silvicolum may not be roost‐limited on BCI in spite of its highly specialized roost choice.     

Niche overlap and trophic resource partitioning of two sympatric batoids co‐inhabiting an estuarine system in southeast Australia

Elasmobranchs play an important role within the trophic structure of marine ecosystems, but there are relatively few studies published on the feeding ecology of these species. Reported herein is the feeding ecology and trophic resource partitioning of two sympatric batoid species, Urolophus cruciatus and Narcine tasmaniensis from southeast Australia. The diet of males and females of both species was similar, suggesting no sex‐specific dietary preferences. Ontogenetic changes in diet were observed from the diets of both species: as the body size increased, the proportion consumed of crustacea to polychaeta decreased. A relatively high degree of niche overlap (70%) was detected between the trophic resources of the two species. The way in which the predators partitioned the resources, however, was significantly different. U. cruciatus fed predominately on small benthic crustaceans (amphipods and decapods), while N. tasmaniensis displayed a preference towards Maldanidae polychaetes. Therefore, although U. cruciatus and N. tasmaniensis both feed predominately on benthic invertebrates, they specialise on different taxa. This trophic resource partitioning contributes to the biodiversity of the region by facilitating the coexistence of these sympatric species.